Epidemiology of Split Cord Malformations

Although their precise incidence is unknown, SCMs are exceedingly rare and represent 3.8% to 5% of all congenital spinal anomalies.^3,5 One recent series estimated the prevalence of SCM to be 1 in 5000 (0.02%) live births.⁶ Similar to other forms of occult spinal dysraphism, there is a slight female preponderance, approximately 1.3:1.^7–10 The peak age at initial medical evaluation is 4 to 7 years, although there is a second peak between 12 and 16 years of age coinciding with the postpubescent growth spurt. A delay in diagnosis until adulthood may be seen, with back pain being the sole complaint^7,8,10,11 or pain accompanied by progressive neurological deficits that may be mistaken for degenerative disease. Although estimates of prevalence vary, type I SCMs may occur more frequently than type II lesions.^8,10,11

SCMs rarely occur in the absence of associated anomalies. The most common associations (in descending order) are a tethered/low-lying cord (>50%), kyphoscoliosis (44% to 60%), syringomyelia (27.5% to 44%), and spina bifida (11% to 26%).^7,8,10 Conversely, SCMs may occur in 5% of patients with congenital scoliosis¹² and in up to 15% of patients with myelomeningocele.^13,14 When SCM is seen in association with myelomeningocele, it is three to four times more likely to be a type I malformation and tends to occur at or just rostral to the level of the myelomeningocele defect. On occasion, multiple dysraphic lesions may be identified, and occult SCMs can account both for a discrepancy between functional level and anatomic level of the myelomeningocele placode and for late neurological deterioration in patients with myelomeningocele and an undisclosed SCM.¹¹ Dermoids, dermal sinus tracts, and neurenteric cysts may also be found in conjunction with SCMs.

Embryogenesis

SCMs are thought to occur during the third week of embryogenesis, concurrent with gastrulation, as a result of failure of fusion of the notochord in the midline and subsequent persistence of an accessory neurenteric canal.^1,3,15,16

On day 17 of human development, cells of Hensen’s node ingress at the embryonic midline to begin formation of the notochord. In a process of cell-to-cell intercalation, bilayers of cells ingress from each side of midline and intermix to form a singular midline notochordal process.¹⁷ Oriented cellular division and cell-to-cell intercalation contribute equally to the process of convergent extension by which the notochord elongates. Oriented cellular division refers to the preferential direction of mitosis demonstrated during embryogenesis that allows a mass of cells to extend in a particular plane rather than growing spherically. Intercalation refers to the cellular process by which two groups of cells integrate in a mosaic pattern (Fig. 216-2A). Thus, polar integrated growth of the combined mass occurs in the cranial-caudal direction. Cellular intercalation is partially governed by genes of the wnt family, which are also responsible (along with sonic hedgehog) for dorsal-ventral patterning of the vertebrate nervous system.¹⁸ Knockouts of Prickle, another cell polarity molecule that is conserved across species, demonstrate a foreshortened and thickened notochord.

FIGURE 216-2 A, Normal development of the notochord by intercalation of two paramedian cell masses at Hensen’s node. B, Delayed integration of the paramedian cell masses results in a split notochord and persistent adhesion of the ectoderm and endoderm, which is thought to underlie both types of split cord malformation.

(Original sketches provided by Andy Rekito, M.S., Oregon Health & Science University.

Reciprocal induction of notochordal and paraxial mesodermal cells also plays a key role in this process. Mesodermal somites express protocadherin, which promotes midline intercalation of the notochord. Embryos lacking protocadherin demonstrate normal elongation of the paramedian notochord masses but no integration, reminiscent of the failed integration seen over small spinal segments in human SCM¹⁹ (Fig. 216-2B). Once formed, the notochord acts as an organizer by secreting multiple morphogens that are responsible for proper neurulation of the embryo. Experimental transplantation of notochord fragments has demonstrated that presence of the notochord is necessary and sufficient to influence patterning of spinal development²⁰ and that ectopic or redundant notochordal tissue may result in complete duplication of the spinal cord and surrounding tissues.²¹ Emura and colleagues produced an amphibian model of SCM by microsurgically creating a neurenteric fistula in embryos, which were then incubated to term. They observed SCM in 40% of the embryos that survived the procedure.²²

Most theories posit two common prerequisites for the development of SCM.1,3,23^,24 The first is persistent adhesion of the ectoderm and endoderm, termed an accessory neurenteric canal by Bremer.²⁴ The second is a cleft notochord, with subsequent induction of a cleft spinal cord. In 1992, Pang proposed a unified theory for the development of both types of SCM in which these two prerequisites occur as the result of a single ontogenic event—failure of midline integration of the anlagen destined to become the notochordal process.³ This theory postulates that the mass of cells derived from the primitive pit does not ingress as a single mass but instead exhibits left-right asymmetry whereby it courses mediolaterally from the primitive pit before reintegrating in the midline (Fig. 216-2B). Failure of reintegration leads to the formation of an accessory neurenteric canal, which Pang labeled the endomesenchymal tract.¹¹ Persistence of the endomesenchymal tract results in a median cleft with two heminotochords, which induces a similarly cleft spinal cord.

This unified theory explains the subsequent occurrence of types I and II SCM based on incorporation of the meninx primitiva into the endomesenchymal tract. Inclusion of meninx primitiva cells, which arise around day 30, results in the formation of two completely separate dural sleeves as seen in a type I SCM. Inasmuch as the meninx primitiva is osteogenic, this also results in the formation of a midline bony spur (see Fig. 216-1A). When the meninx primitiva is not incorporated into the endomesenchymal tract, a single dural sleeve (and single arachnoid space) contains two hemicords separated by a thin fibrous band, as seen in a type II SCM (see Fig. 216-1B). Incorporation of neural crest (other than the meninx primitiva) into the endomesenchymal tract results in the formation of neural elements medial and dorsal to the hemicords that extend to the extradural space and result in the formation of dorsal bands.

The presence of two separate notochordal anlagen during formation of the notochordal process has never been directly observed, but knockout mice lacking genes for intercalation develop two heminotochords that are not fused in the midline.¹⁹ The unified theory suggests that caudal failures of midline integration, which occur relatively late during embryonic development, are more likely to coincide with emergence of the meninx primitiva and thus produce type I SCMs. In fact, type I SCM most frequently occurs from L2 to L4 and is rarely seen above the thoracolumbar junction, whereas type II SCM occurs almost exclusively above T8.⁸

Signs and Symptoms

Patients with split cord may be asymptomatic, with only cutaneous stigmata of their spinal dysraphism. In various series, there is some type of cutaneous mark present in up to 92% of patients.^{7,10,11,14,25} The common stigmata associated with SCM are summarized in Table 216-2.^{7–11,14,25,26} Because of the rostral migration of neural elements relative to the bony spinal column that normally occurs after the formation of an SCM, cutaneous markers are found somewhat caudal to the level of the neural defect itself. The presence of hypertrichosis, although variable, is highly specific for SCM (Fig. 216-3A). One report identified an odds ratio of 61.6:1 in favor of the occurrence of an SCM if a hairy patch is present.²⁵ One characteristic variation of hypertrichosis, the “faun’s tail,” consists of a patch of unusually coarse, raised hair that is strongly associated with type I SCM.²⁵ There is typically a capillary hemangioma underlying these hairy patches. On occasion (≈7%), hemangiomas alone, without overlying hypertrichosis, may indicate the presence of an SCM. Although sacral dimples, dermal sinuses, and cutaneous lipomas are not specific to SCM per se, they often indicate the presence of an additional underlying dysraphic lesion in a patient with SCM (Fig. 216-3B). True sacral dimples that are suggestive of underlying dysraphism should be distinguished from shallow, symmetrical dimples over the coccygeal midline. The latter is common in the general population and is not indicative of the presence of distal tethering pathology.

TABLE 216-2 Clinical Signs and Symptoms

FIGURE 216-3 A, A typical patch of coarse, pigmented hair indicates the presence of a split cord malformation (SCM). B, A patch of coarse hair with atretic skin indicates the presence of an SCM, and a prominent sacral dimple (arrow) indicates the presence of an associated fatty filum terminale.

A majority of patients with SCM have one or more signs and symptoms of neurological deterioration.¹¹ Axial back pain is common and is typically focal and intense around the levels of the split cord. Adults with undiagnosed SCM may have back pain as the only symptom. A radicular component may be present in 10% of both adult and pediatric patients.^10,25

Progressive sensory or motor dysfunction (or both) is seen in two thirds of patients. There are two separate, but interrelated causes of asymmetrical motor findings in the lower extremities. Nearly 50% of patients have gross (i.e., structural) asymmetry of the lower extremities, a condition referred to as neuro-orthopedic syndrome. This syndrome is characterized by a triad of limb length discrepancy, muscular atrophy (resulting in secondary weakness), and clubfoot deformity (talipes equinovarus).^27–29 The smaller limb is often ipsilateral to a smaller hemicord. Fewer patients (about ≈20%) have an asymmetrical neurological deficit despite structural symmetry of the limbs. This finding is highly associated with hydromyelia of one hemicord.⁸

Autonomic dysfunction is typically manifested as urologic signs and symptoms. Subjective complaints of enuresis are a poor indicator in comparison to objective urodynamic testing. Although only about one third of patients typically have complaints of urinary dysfunction, urodynamic studies demonstrate abnormal bladder function in nearly three quarters.²⁶ Detailed urologic assessment should be undertaken as part of the initial evaluation and before any surgery.

Surgeons evaluating a patient for suspected SCM should be cognizant of associated anomalies that may require additional surgical intervention. Summarized in Table 216-3,^7,8,10 associated anomalies include scoliosis, tethered cord secondary to a thickened filum or terminal lipoma, myelomeningocele (with associated Chiari II malformation), and syringomyelia.

TABLE 216-3 Associated Anomalies

Data from references 7, 8, and 10.

Imaging

Magnetic resonance imaging (MRI) has led to significant advances in the preoperative diagnosis and planning for surgical management of SCM. The cardinal feature on MRI is the presence of two hemicords, which are best visualized on T1-weighted sequences (Fig. 216-4). The cleft typically begins below T11 and the hemicords most often reunite after two to three vertebral segments.^8,30 T1-weighted images are also helpful in demonstrating the presence of an associated fatty filum, which may affect one or both hemicords, a dermal sinus tract, or a terminal lipoma (Fig. 216-5). Associated tethering anomalies are present in approximately half of all patients and in more than 90% of those with a low-lying conus.^10,11 T2-weighted MRI typically discriminates between the presence of one or two subdural and subarachnoid spaces, which allows proper categorization of the malformation as type I or type II (Fig. 216-6). T2-weighted axial and coronal images may also demonstrate a hypointense fibrous band in type II SCM. In nearly half of all cases, T2-weighted images also demonstrate syringomyelia proximal to the cleft, which may extend into one or both hemicords³⁰ (Fig. 216-7). Because multiple, often redundant tethering elements may be present at the level of the SCM and elsewhere, careful inspection of the entire spinal intradural space should be undertaken with MRI. Unlike the situation in patients with open dysraphic conditions, brain imaging is not automatically required.

FIGURE 216-4 Axial T1-weighted magnetic resonance image demonstrating a type II split cord malformation, characterized by two hemicords in single dural sac.

FIGURE 216-5 A, Axial T1-weighted non–contrast-enhanced MRI scan demonstrating tissue with high signal intensity (arrows) representing the fatty fila of each hemicord. B, Sagittal T1-weighted non–contrast-enhanced MRI scan demonstrating a terminal lipoma (arrow) in the same patient. C, Intraoperative view (same patient) documenting the duplicated fatty fila and a terminal lipoma (arrow).

FIGURE 216-6 A, Axial T2-weighted MRI scan demonstrates duplicated subarachnoid spaces in a type I split cord malformation (SCM). B, By contrast, axial T2-weighted MRI scan shows a single subarachnoid space in a type II SCM.

FIGURE 216-7 Sagittal T2-weighted MRI scan demonstrating hydromyelia (arrow) of the normal spinal cord craniad to the level of a split cord malformation.

In type I malformations, computed tomography (CT) best delineates the configuration of the osseous spur. Most spurs occur as a midline bony outgrowth of the posterior aspect of the vertebral body, although spurs with oblique orientation and spurs arising from the neural arch have been reported⁵ (Fig. 216-8). SCM is associated with bony anomalies in more than 85% of patients.⁵ The more common bony segmentation defects include bifid vertebrae, bifid laminae, Klippel-Feil malformation, butterfly vertebrae, and hemivertebrae. SCM is associated with scoliosis in 50% to 60% of patients, and SCM is present in 5% of patients with congenital scoliosis.^2,31 The apex of the major curvature generally coincides with the level of the SCM because of a strong association of segmentation and vertebral body defects at that level.⁸ Both tethering and congenital vertebral anomalies contribute to the formation and progression of scoliosis. The scoliotic component may best be appreciated on coronal images from MRI, CT, or standing plain films. Based on published series, CT myelography is superior to MRI in detecting the bony septum of type I SCM (100% versus 82%), bifid vertebrae (100% versus 65%), and hypertrophic neural arches (100% versus 54%).⁸ Complex, hypertrophic neural arches are seen most often with type I malformations, presumably because of the presence of additional osteogenic meninx primitiva during development. Hypertrophic arches are often fused to the lamina of an adjacent segment, a condition referred to as intersegmental laminar fusion. When associated with bony spina bifida (60% of cases), this finding is virtually pathognomonic for type I SCM³¹ (Fig. 216-9).

FIGURE 216-8 Axial non–contrast-enhanced CT scan demonstrating a bony spur arising from the neural arch and associated with a split cord malformation.

FIGURE 216-9 Three-dimensional CT reconstructions of the spine from a patient with a split cord malformation (SCM) and scoliosis. A, An anterior view demonstrates fusion at T6/7 (white arrow) coinciding with the apex of the scoliotic curve. Note the butterfly vertebra at T10 (black arrows). B, The posterior view demonstrates intersegmental laminar fusion at T6/7 (white arrow) and spina bifida occulta of the adjacent segments (black arrows). This combination of findings is virtually pathognomonic for type I SCM.

Overall, CT and MRI are complementary imaging modalities that provide information critical for the management of patients with SCM. MRI is an excellent screening tool that allows identification of the malformation and associated tethering anomalies without exposing the patient to radiation. Given the high incidence of associated bony abnormalities and their influence on surgical planning, performance of non–contrast-enhanced CT with sagittal and coronal reconstructions is often helpful. CT myelography is not necessary unless the patient has a condition preventing high-resolution MRI. Plain film radiographs may be useful for the long-term follow-up and management of associated scoliotic deformities, as well as for the identification of bony landmarks during surgery.

Surgical Management

The mere presence of a type I SCM is often taken as indication for operative intervention. A unique, but small long-term natural history study in patients with type I SCM from the early 1970s observed that 85% of patients without intervention suffer from a progressive neurological deficit versus only 4.5% after surgical treatment.²⁷ Pang observed a similarly high rate of progressive neurological deterioration in patients with type II as with type I SCM and therefore advocated “prophylactic” surgical exploration of both types of malformation.⁸ By contrast, many surgeons elect to serially observe neurologically and urologically asymptomatic patients with type II SCM discovered incidentally or as a result of the presence of a cutaneous marker only. Unfortunately, data on the long-term natural history of type II SCM and contemporary long-term data from the MRI era regarding type I SCM are not available.

When undertaken, the principal goal of surgery is to untether the spinal cord by operative management of both the SCM and any associated tethering anomalies. Surgical repair of SCM is often performed in conjunction with intraoperative electrophysiology, including continuous somatosensory evoked potential monitoring of the extremities at and below the malformation, motor evoked potential monitoring, or electromyography and anal sphincter monitoring (or any combination of these studies). The patient is positioned prone after a Foley catheter is placed. Intraoperative fluoroscopy can be helpful in localizing the level of the SCM and defining any associated abnormal bony anatomy, especially because cutaneous stigmata may lie caudal to the actual level of the SCM. In type II SCM, the associated neural arch anomalies may not provide any obvious intraoperative anatomic landmarks.

Care must be taken during midline exposure to avoid durotomy and neural injury given the high incidence of concomitant neural arch defects. The complex bony anatomy associated with the SCM may be correlated with preoperative and intraoperative bone imaging. Exposure generally extends one to two levels above and below the SCM to allow dissection to extend from normal to abnormal anatomy. At this point, operations for types I and II SCM differ significantly. For type I SCM, the initial laminectomies should be limited to adjacent levels while initially avoiding exposure of dura at the level of the midline bony spur. Rongeurs or a high-speed drill (or both) should then be used to perform bilateral paramedian laminectomies while preserving the midline lamina and spinous process and thus preventing any torque or lateral force from disrupting the bony spur prematurely.¹¹ Once the spur is isolated and exposed, blunt subperiosteal dissection may be performed to separate the dural sleeves from the spur bilaterally. Dissection typically occurs in a rostral to caudal fashion—from the least adherent to the most adherent dura. Once freed, the spur may be resected carefully with a small rongeur or high-speed drill. Significant bleeding may occur from medullary vessels within the spur itself and can often be controlled with bone wax. Bone removal is complete when the spur is flush with the posterior wall of the vertebral body.

All bone work should be completed before opening the dura. Under magnification, the dura is opened sharply in the midline above and below the lesion and on either side of the split at the level of the duplicated dural sleeves. Sharp dissection can be used to free the hemicords from their medial attachments to the dural sleeves. Typically, these attachments are either coalescent arachnoid bands, similar to the dentate ligament, or dorsal paramedian, nonfunctional nerve roots that end blindly in the dura and are generally most dense and tenacious at the caudal end of the defect where they abut the bony spur directly. These paramedian roots may extend through the dura with a fibrovascular tuft. Once freed, the central dura can be sharply resected to the level of the posterior longitudinal ligament ventrally to restore the normal configuration of a single thecal sac.

Care should also be taken when removing lamina at the level of the SCM in type II malformations because of the frequent presence of transdural adhesions. Often, the dura at this level will appear grossly abnormal. A single midline dural opening traversing the fibrous bands at the level of the SCM should be made sharply. These bands are most commonly attached to the dura dorsally but may also attach ventrally. All non-neural and nonfunctional adhesive bands should be transected, beginning dorsally and then gently rolling the hemicords to one side and transecting any ventral attachments. These bands may be invested with prominent vasculature that requires careful management. In type II SCM, the hemicords are typically closely approximated with no clear intervening plane. Resection of the fibrous band within the split spinal cord itself is not indicated.

Any associated tethering lesion (sinus tract, fatty filum, or terminal lipoma) should also be addressed. Most authors advocate sectioning of a normal filum in all patients with a low-lying conus.⁷ Distal tethering of the conus is nearly always present in patients with lower thoracic and lumbar SCMs and, although less frequent, cannot be excluded even in those with more cranially located malformations.⁸ Dorsal bands are seen with equal frequency in type I and type II malformations and represent an additional tethering lesion.⁷ Depending on the location of the SCM, distal untethering and treatment of the SCM itself may be undertaken through a single or through two separate incisions. Any additional tethering bands should also be transected so that both hemicords and the conus can move freely within the spinal canal. Successful untethering often indirectly treats syringomyelia effectively. Large, progressive, or recurrent syringes, however, may require direct surgical management. Dorsally, the dura is closed in watertight fashion, if necessary, with a dural patch. One potential advantage of expansion duraplasty is that it discourages retethering. Anterior dural defects are rarely the source of a cerebrospinal fluid (CSF) leak and are not typically closed.

Patients should be kept flat postoperatively for 1 to 2 days to allow a preliminary seal to form along the dural suture line. Some surgeons prefer to maintain patients in the prone position during this initial recovery to discourage adhesion of the spinal cord to the dural closure site. The Foley catheter is removed at the time of mobilization, with monitoring of postvoid residuals. Transient urinary retention affects up to 20% of patients and may require intermittent straight catheterization or discharge with a Foley catheter temporarily in place.³²

Outcomes

Surgical repair of SCMs results in improvement or stabilization of progressive neurological deficits in more than 90% of patients.^7–1133 Functional outcomes are summarized in Table 216-4.^7–10 Axial back pain is improved in the majority of patients and otherwise generally decreases to a tolerable level.⁸ The remainder of symptoms can be conveniently divided among motor, sensory, and autonomic (bladder) dysfunction. Progressive sensory and motor deficits show the most pronounced improvement after surgical intervention.⁹ Up to one third of patients will regain urinary function postoperatively.⁷ The extent of neurological and urologic recovery is related in part to the timing of intervention. Outcomes are most favorable in asymptomatic patients identified by cutaneous stigmata—with most series describing complete preservation of neurological function in patients in whom prophylactic repair is undertaken.^7,8 A stable neurological state may in some cases persist for decades, and perhaps indefinitely, after surgical SCM repair.³⁴

TABLE 216-4 Outcomes After Surgical Intervention for Split Cord Malformation

Data from references 7–10.

Complications associated with repair of SCM include CSF leak, wound infection, and new neurological deficits (Table 216-5).^7–1132 Secondary repair of an SCM in a patient with a previously closed myelomeningocele at the same level carries a risk for failed wound healing as high as 10%.^7,14 Transient urinary retention is the most common new neurological deficit and is seen in up to 25% of patients.³² New sensorimotor deficits may develop in 7% of patients. The majority of these deficits are transient; however, there is a 3% incidence of new permanent deficits.^7–11

TABLE 216-5 Complications After Surgical Intervention for Split Cord Malformation

Data from references 7–11 and 32.

If possible, pediatric patients with SCM should be monitored after their primary repair by an interdisciplinary spina bifida care team, including members of pediatrics, pediatric neurosurgery, orthopedics, physical therapy, and pediatric urology. Recurrence of symptoms or delayed onset of new deficits may be due to retethering, sometimes associated with scarring at the surgical site, or to a previously undiagnosed secondary lesion. Because asymptomatic changes in bladder detrusor function may be an early sign of retethering, occasional urodynamic bladder testing may be useful. Repeat imaging often demonstrates the appearance of anatomic tethering after surgical repair of an SCM, even in asymptomatic patients. Thus, radiographic demonstration of a persistent low-lying cord in an asymptomatic patient should not be taken as an indication for reoperation. MRI is useful in the evaluation of symptomatic patients for retethering by demonstrating the appearance or enlargement of syringomyelia, which provides independent evidence of clinical worsening, or the presence of an additional, previously unrepaired tethering element. Ultimately, the diagnosis of retethering is made on clinical grounds.

Conclusion

SCMs are a rare form of congenital spinal malformation that shed light on the development of the vertebrate spinal cord. Both types I and II SCM appear to arise from the same developmental anomaly and result in mechanical tethering of the spinal cord. Earlier surgical intervention for SCM is associated with better long-term functional outcome. For this reason, diagnostic imaging is indicated for children with associated cutaneous and orthopedic signs of SCM or progressive neurological or urologic deficits (or both). Because SCMs are often associated with additional tethering lesions, MRI before surgical intervention should include the entire spine through the craniocervical junction. Operative repair is generally undertaken in patients with either symptomatic or asymptomatic type I SCMs, given the high risk for progressive neurological and urologic deficits associated with this condition, even in those with initial intact function. The goal of surgery is to halt or prevent progression of motor, sensory, and bladder dysfunction and, when possible, to improve any initial signs and symptoms. Regular postoperative follow-up should ideally include interdisciplinary evaluation by a clinical spina bifida team. Early diagnosis, meticulous surgical care, and careful follow-up offer the possibility of preserving or restoring normal function in many children and adults.